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Published on November 3, 2006; 10.1104/pp.106.090050

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Received September 19, 2006
Accepted October 24, 2006

A Phytophthora Infestans Cystatin-like Protein Targets a Novel Tomato Papain-like Apoplastic Protease

Miaoying Tian , Joe Win , Jing Song , Renier van der Hoorn , Esther van der Knaap , and Sophien Kamoun *

Department of Plant Pathology, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, OH 44691, USA
Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany
Department of Horticulture and Crop Sciences, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, OH 44691, USA

* Corresponding author; email: kamoun.1{at}osu.edu.

There is emerging evidence that the proteolytic machinery of plants plays important roles in defense against pathogens. The oomycete pathogen Phytophthora infestans, the agent of the devastating late blight disease of tomato and potato, has evolved an arsenal of protease inhibitors to overcome the action of host proteases. Previously, we described a family of fourteen Kazal-like extracellular serine protease inhibitors from P. infestans. Among these, EPI1 and EPI10 bind and inhibit the pathogenesis-related (PR) P69B subtilisin-like serine protease of tomato. Here, we describe EPIC1-EPIC4, a new family of P. infestans secreted proteins with similarity to cystatin-like protease inhibitor domains. Among these, the epiC1 and epiC2 genes lacked orthologs in Phytophthora sojae and Phytophthora ramorum, were relatively fast-evolving within P. infestans, and were upregulated during infection of tomato, suggesting a role during P. infestans-host interactions. Biochemical functional analyses revealed that EPIC2B interacts with and inhibits a novel papain-like extracellular cysteine protease, termed Phytophthora Inhibited Protease 1 (PIP1). Characterization of PIP1 revealed that it is a PR protein closely related to Rcr3, a tomato apoplastic cysteine protease that functions in fungal resistance. Altogether, this and earlier studies suggest that interplay between host proteases of diverse catalytic families and pathogen inhibitors is a general defense-counterdefense process in plant-pathogen interactions.




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